Transactions of the Royal Society of Tropical Medicine and Hygiene (2008) 102/S1, S26 S29 available at www.sciencedirect.com
j o u r n a l h o m e p a g e : w w w . e l s e v i e r h e a l t h . co m / j o u r n a l s /t r s t
Melioidosis and Aboriginal seasons in northern Australia Allen C. Chenga,b, *, Susan P. Jacupsb , Linda Wardb,c , Bart J. Currieb,c a
Department of Medicine, University of Melbourne, c/o Victorian Infectious Diseases Service, 9th floor, Royal Melbourne Hospital, Grattan Street, Parkville, VIC 3052, Australia b Menzies School of Health Research, Charles Darwin University, Darwin, NT, Australia c Northern Territory Clinical School, Flinders University, Darwin, NT, Australia
KEYWORDS Melioidosis Burkholderia pseudomallei Seasonal variation Traditional knowledge Aborigine Australia
Summary Melioidosis, an infection due to the environmental bacterium Burkholderia pseudomallei, is endemic to Southeast Asia and northern Australia, with cases strongly correlated with the monsoonal wet season. We hypothesized that seasonal variation in the mode of acquisition, informed by traditional knowledge, would result in variations in disease characteristics as well as disease incidence. We explored the seasonal variation in acute, cultureconfirmed melioidosis using local Aboriginal definitions of seasons in presentations to the Royal Darwin Hospital, the referral centre for the Top End of the Northern Territory, Australia. In 387 patients, we observed an increased proportion of patients with pneumonia (60%) and severe sepsis (25%) associated with presentations in the wet seasons Gunumeleng (October December) and Gudjewg (January March) compared with the drier seasons Wurrgeng (June August) and Gurrung (August October) (pneumonia 26%, severe sepsis 13%). This observation supports the hypothesis that in the wet seasons there may be changes in the mode and/or magnitude of exposure to B. pseudomallei, with a shift from percutaneous inoculation to aerosol inhalation, for instance. © 2008 Published by Elsevier Ltd on behalf of Royal Society of Tropical Medicine and Hygiene.
1. Introduction Melioidosis is an infectious disease associated with exposure to mud and pooled water. 1 Infections may be protean; they may affect any organ in the body, but primarily the lungs and the intra-abdominal organs. Although incubation periods as long as 62 years have been described, 2 it is believed that most cases occur within 1 d to 2 3 weeks after exposure, 3 with a spectrum of severity ranging from overwhelming sepsis to skin lesions or more chronic disease. Aboriginal culture is closely linked to the environment, with cultural beliefs and practices tied to the availability of seasonal food sources, water and accommodation. 4 In addition, seasonal practices such as lighting fires are believed to result in sustainable environmental practices. 5 Apart from meteorological conditions, other factors such as the behaviour of native flora and fauna, determine the passage of seasons; for example, the appearance of dragonflies in April usually signals the end of the monsoonal rains. * Corresponding author. Tel.: +61 3 9342 7212; fax: +61 3 9342 7277. E-mail address:
[email protected] (A.C. Cheng). 0035-9203/ $
The correlation between rainfall and the incidence of melioidosis has been well described. 3,6 8 We hypothesized that changes in weather patterns and behaviours associated with each season, informed by traditional knowledge, may result in a different mode and magnitude of exposure to Burkholderia pseudomallei, with a consequent change in the pattern and severity of disease and not only the incidence of disease.
2. Materials and methods We considered acute culture-confirmed cases of melioidosis that presented to the Royal Darwin Hospital during the period of January 1990 to March 2007. Patients were included if they resided within the endemic area within the Northern Territory and were identified as from rural areas if their place of residence was outside urban Darwin/Palmerston or Katherine. We considered the first episode of illness for each patient, excluding recurrent disease. Pneumonia was defined by radiological evidence of consolidation supporting a clinical diagnosis. Severe sepsis was defined by standard criteria. 9 Mortality was defined as death attributable to
see front matter © 2008 Published by Elsevier Ltd on behalf of Royal Society of Tropical Medicine and Hygiene.
Melioidosis and Aboriginal seasons in northern Australia
S27
Fig. 1. Map of Top End of Northern Territory, Australia.
acute infection during the hospital admission. Aboriginality was assessed by self-identification. The traditional owners of the Kakadu Region (Figure 1), the Bininj/Mungguy people, recognize six distinct seasons in this area, known as the Gundjeihmi calendar (Figure 2). 4,10 Gunumeleng, occurring between October and late December, is the hot, pre-monsoonal season. It is known colloquially as the ‘build up’, becoming increasingly humid and uncomfortable. Thunderstorms often occur later in the day and are associated with scattered showers. Traditionally, Aboriginal people moved camp from the floodplain to the higher ‘stone country’ in preparation for the monsoonal rains. Gudjewg, from January to March, is associated with violent thunderstorms, heavy rain and flooding. Heat and humidity are associated with an increase in plant and animal life. Banggereng, in April, is also known as the time of sudden, isolated ‘knock’em down’ storms. During this time floodplains begin to recede and streams run. Yegge, in May to mid-June, is associated with dry winds. Fires are traditionally lit during this time to ‘clean’ the country, prevent destructive fires later in the year and encourage new growth for grazing animals. The colder Wurrgeng, from mid-June to mid-August, is characterized by low humidity and progressively drier land. Waterfowl are more concentrated in the diminishing water areas. Gurrung, from mid-August to October, is windless and increasingly warm. Seasonality was tested using the exact Walter Elwood test. In this statistical test, a harmonic curve is fitted to data, with both variations in the duration of seasons and the number of total cases in each season taken into account. The null hypothesis was that the proportion of disease occurring in each season with a particular presentation is the same. To test monthly variation in the number of cases
of melioidosis, the Edwards test, which does not account for variations in the population at risk, was used. Statistical tests were performed using the seast module (Pearce MS, Feltblower R, STB-56) on Stata 9.0 (Stata Corp., College Station, TX, USA).
3. Results During the study period, 387 patients presented with acute culture-confirmed melioidosis. The majority of cases (88%) occurred in the monsoonal wet seasons Gunumeleng, Gudjewg and Banggereng (October to March). Overall, 15% of patients died due to acute illness, 53% of patients had pneumonia, 20% of patients had genitourinary disease, 60% of patients were bacteraemic and 25% of patients had severe sepsis. There was a change in the pattern of disease with a general increase in the proportion of pneumonia and severe sepsis and attributable case-fatality during Gunumeleng and Gudjewg (Figure 2). Conversely, the drier seasons Wurrgeng and Gurrung were associated with a lower proportion of patients with pneumonia and severe sepsis and a high proportion with genitourinary disease. When analysing clinical parameters by season, only the seasonal variation in mortality and pneumonia were statistically significant (Table 1). A greater amplitude of cyclic variation was noted for mortality, pneumonia, genitourinary disease and severe sepsis for Aboriginal patients (n = 204; 53%) and patients from rural areas (n = 181; 47%) (Table 1). There was no obvious variation in the proportion of bacteraemia with season.
4. Discussion In all cultures, changes in the weather and environment have effects on behaviour. In some areas where melioidosis
S28
A.C. Cheng et al. J
F
M
A
M
J
J
A
S
O
N
D
Month
Banggerreng Gudjewg
Yegge
Wurrgeng
Gurrung
Gunumeleng
Season
0.8 0.7 0.6 0.5
Died
0.4
Bacteraemic
0.3
Severe sepsis
0.2 0.1 0
0.7
250
0.6
200
0.5 0.4
150
0.3
100
Total Pneumonia
0.2
Genitourinary
50
0.1 0
0
Fig. 2. Proportion (left axis) and number of presentations (right axis) with melioidosis in each Gundjeihmi Aboriginal season. Table 1
Seasonal variation in numbers of patients with melioidosis and disease characteristics Amplitude of cyclic variation (P value) by season
Aboriginal patients (n = 204) by season
Rural patients (n = 181) by season
All patients (n = 387) by month No. of cases a
1.48 (<0.001)
Melioidosis-attributable mortality
0.47 (0.09)
0.57 (0.03)
1.1 (0.001)
0.84 (0.03)
Pneumonia
0.37 (0.005)
0.38 (0.005)
0.67 (<0.001)
0.53 (0.009)
Genitourinary disease
0.19 (0.57)
0.22 (0.49)
0.55 (0.09)
0.27 (0.54)
Bacteraemia
0.13 (0.49)
0.14 (0.44)
0.08 (0.83)
0.18 (0.48)
Severe sepsis
0.25 (0.30)
0.24 (0.37)
0.45 (0.12)
0.31 (0.40)
a
Edwards test for seasonality of number of cases; other characteristics, Walter Elwood test for seasonality in proportions.
is endemic, such as Thailand, the incidence of the water-associated diseases melioidosis and leptospirosis is associated with occupational exposure to flooded rice paddies during planting and harvesting. 11 In Australia, Aboriginal patients comprise approximately half the cases of melioidosis in northern Australia but only 25% of the population of the region. 12 Although only a proportion of Aboriginal patients live traditionally, we recognize that changes in the environment influence all people resident in the region to some extent. We chose to explore the association between seasonal weather changes and melioidosis using Aboriginal seasons because the definitions of the seasons were more closely associated with weather changes in tropical northern Australia
than traditional European season definitions developed in more temperate climates. Although changes in the seasons may vary from year to year, the data we present support an association between the wet seasons and melioidosis presenting as pneumonia in comparison with melioidosis presentations in the drier seasons. These manifestations were in contrast to genitourinary disease, which tended to increase in the drier seasons as the proportions with other manifestations of melioidosis fell. The lack of statistical significance in parameters other than pneumonia may well reflect the relatively smaller numbers of patients with severe sepsis and genitourinary disease. Analyses of the subgroup of Aboriginal ethnicity and patients from rural areas should be interpreted with caution due to smaller
Melioidosis and Aboriginal seasons in northern Australia numbers. In these patients there was, however, a trend for greater seasonal association of pneumonia, consistent with them being exposed to a possibly larger impact of the seasonal effects on melioidosis presentations. Greater power would be expected if seasonal variation was examined in Thai patients. However, although tropical, the weather conditions in the endemic area of inland northeast Thailand are significantly different from those of coastal Australia. Furthermore, the association between climate and melioidosis in Thailand is confounded by agricultural practices to a far greater extent than in Australia. Although it is possible that cases in the drier seasons may reflect a different pattern of disease associated with a longer incubation period, this change in the proportion of patients with pneumonia may reflect both changes in the mode of acquisition and magnitude of exposure to B. pseudomallei. This reinforces previous work that demonstrates an association between the intensity of rainfall and the incidence of pneumonia and severe sepsis, 7 and an association between disease incidence and extreme weather events. 13 We have suggested that this may well reflect a shift in the mode of transmission from percutaneous inoculation to inhalation of aerosolized bacteria during these times. 7 Alternatively, seasonal climatic changes at this time may encourage the proliferation of B. pseudomallei in pooled water and mud, leading to exposure to higher bacterial numbers and hence a larger inoculating dose. The importance of a shift to inhalation is that this mode of infection is generally associated with more severe disease and far higher mortality than occurs with percutaneous inoculation, analogous to inhalational anthrax, plague and tularaemia. 7 Previous work has also shown that case-clusters of melioidosis in humans and animals are associated with localized anthropogenic environmental change such as soil disturbance from construction work. 14,15 In addition, there are implications for melioidosis in the predictions that global climate change will result in more severe weather events such as cyclones in tropical regions. In conclusion, further surveillance is needed to monitor changes in the epidemiology of melioidosis with future regional changes in environment and climate. This will help unravel the complex relationships of melioidosis incidence and disease presentations with anthropogenic environmental change from both agricultural and construction, anthropogenic climate change and natural seasonal cycles such as those articulated by Indigenous populations. Authors’ contributions: ACC and BJC conceived the study design; ACC performed the initial analysis with support from SPJ and LW. All authors contributed to the writing of the manuscript and read and approved the final version. BJC is guarantor of this paper. Funding: AC is supported by an NHMRC postdoctoral fellowship. This project is supported by an NHMRC project grant. Conflicts of interest: None declared.
S29 Ethics approval: Ethical approval for clinical studies in melioidosis has been granted by the Human Research Ethics Committee of the Department of Human Services and the Menzies School of Health Research, Australia.
References 1. Cheng AC, Currie BJ. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 2005;18:383 416. 2. Ngauy V, Lemeshev Y, Sadkowski L, Crawford G. Cutaneous melioidosis in a man who was taken as a prisoner of war by the Japanese during World War II. J Clin Microbiol 2005;43:970 2. 3. Currie BJ, Fisher DA, Howard DM, Burrow JN, Selvanayagam S, Snelling PL, et al. The epidemiology of melioidosis in Australia and Papua New Guinea. Acta Trop 2000;74:121 7. 4. Press T, Lea D, Webb A, Graham A. Kakadu: Natural and Cultural Heritage and Management. Darwin: Australian Nature Conservation Agency and North Australia Research Unit, Australian National University; 1995. 5. Johnston F, Jacups S, Vickery A, Bowman D. Ecohealth and Aboriginal testimony of the nexus between human health and place. Ecohealth 2007;4:489 99. 6. Chaowagul W, White NJ, Dance DA, Wattanagoon Y, Naigowit P, Davis TM, et al. Melioidosis: a major cause of community-acquired septicemia in northeastern Thailand. J Infect Dis 1989;159:890 9. 7. Currie BJ, Jacups SP. Intensity of rainfall and severity of melioidosis, Australia. Emerg Infect Dis 2003;9:1538 42. 8. Leelarasamee A, Bovornkitti S. Melioidosis: review and update. Rev Infect Dis 1989;11:413 25. 9. ACCP/SCCM. American College of Chest Physicians/Society for Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 1992;20:864 74. 10. Skertchly A, Skertchly K. Traditional Aboriginal knowledge and sustained human survival in the face of severe natural hazards in the Australian monsoon region: some lessons for the past for today and tomorrow. Aust J Emergency Manage 1999;14:42 50. 11. Suputtamongkol Y, Hall AJ, Dance DA, Chaowagul W, Rajchanuvong A, Smith MD, et al. The epidemiology of melioidosis in Ubon Ratchatani, northeast Thailand. Int J Epidemiol 1994;23:1082 90. 12. Currie BJ, Jacups SP, Cheng AC, Fisher DA, Anstey NM, Huffam SE, et al. Melioidosis epidemiology and risk factors from a prospective whole-population study in northern Australia. Trop Med Int Health 2004;9:1167 74. 13. Cheng AC, Jacups SP, Gal D, Mayo M, Currie BJ. Extreme weather events and environmental contamination are associated with case-clusters of melioidosis in the Northern Territory of Australia. Int J Epidemiol 2005;35:323 9. 14. Inglis TJ, Garrow SC, Henderson M, Clair A, Sampson J, O’Reilly L, et al. Burkholderia pseudomallei traced to water treatment plant in Australia. Emerg Infect Dis 2000;6:56 9. 15. Ketterer PJ, Webster WR, Shield J, Arthur RJ, Blackall PJ, Thomas AD. Melioidosis in intensive piggeries in SouthEastern Queensland. Aust Vet J 1986;63:146 9.